Thoracic ultrasound in the modernmanagement of pleural disease

Maged Hassan 1, Rachel M. Mercer2 and Najib M. Rahman2

Affiliations: 1Chest Diseases Dept, Faculty of Medicine, Alexandria University, Alexandria, Egypt. 2OxfordPleural Unit, Oxford Respiratory Trials Unit, University of Oxford, Oxford, UK.

Correspondence: Maged Hassan, Chest Diseases Dept, Faculty of Medicine, Khartoum Square, Alexandria,21521, Egypt. E-mail: magedhmf@gmail.com

@ERSpublicationsWidespread use of US as a point-of-care test has revolutionised the management of pleural diseases. Aonce diagnostic tool for detection of pleural effusion only, the uses of US in pleural diseases haveexpanded to include therapeutics and prognostication. http://bit.ly/2OQQcHZ

Cite this article as: Hassan M, Mercer RM, Rahman NM. Thoracic ultrasound in the modern managementof pleural disease. Eur Respir Rev 2020; 29: 190136 [https://doi.org/10.1183/16000617.0136-2019].

ABSTRACT Physician-led thoracic ultrasound (TUS) has substantially changed how respiratorydisorders, and in particular pleural diseases, are managed. The use of TUS as a point-of-care test enablesthe respiratory physician to quickly and accurately diagnose pleural pathology and ensure safe access to thepleural space during thoracentesis or chest drain insertion. Competence in performing TUS is now anobligatory part of respiratory speciality training programmes in different parts of the world. Pleuralphysicians with higher levels of competence routinely use TUS during the planning and execution of moresophisticated diagnostic and therapeutic interventions, such as core needle pleural biopsies, image-guideddrain insertion and medical thoracoscopy. Current research is gauging the potential of TUS in predictingthe outcome of different pleural interventions and how it can aid in tailoring the optimum treatmentaccording to different TUS-based parameters.

IntroductionThoracic ultrasound (TUS) has become an indispensable tool in the arsenal of the chest physician. The2010 British Thoracic Society (BTS) Pleural Disease Guidelines recommend the use of TUS before pleuralprocedures as a standard of care [1]. Conventionally, TUS has only been used to assess for the presence ofpleural effusion. However, with the widespread availability of TUS machines together with the continuousimprovements in image resolution and the ease these machines can be brought to the bedside and insideprocedure rooms, the use of TUS in thoracic diseases, and particularly in the pleural discipline, hasexpanded substantially. Detailed and advanced examination using TUS supports various diagnostic,prognostic and therapeutic purposes. Ultrasound is an excellent point-of-care test that is now undertakenoutside Radiology departments by physicians from different medical specialities and has become astandard part of training for chest physicians, acting as a much finer adjunct to the stethoscope andclinical examination in guiding clinical decisions.

This review presents a summary of the different evidence-based uses of TUS in the management of pleuraldiseases and how its use enhances safety and accuracy of patient management. The review also provides anoverview of the roles that TUS can potentially contribute, such as favouring pre-procedure probability ofcertain aetiologies and outcome prediction of various interventions in pleural medicine. The advantages ofusing TUS in addition to its pitfalls are summarised in table 1.

Copyright ©ERS 2020. This article is open access and distributed under the terms of the Creative Commons AttributionNon-Commercial Licence 4.0.

This article has supplementary material available from err.ersjournals.com

Provenance: Submitted article, peer reviewed.

Received: 11 Oct 2019 | Accepted after revision: 22 Nov 2019

https://doi.org/10.1183/16000617.0136-2019 Eur Respir Rev 2020; 29: 190136

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Technical aspectsTransducers (probes) emit ultrasound waves with a given frequency and wavelength. These wavespenetrate tissues for variable distances and a portion of these waves are reflected back while the otherportion are absorbed into tissues. The traversing ultrasound waves encounter varying degrees of resistanceaccording to the density of a given medium which leads to some attenuation of the amplitude ofultrasound waves. The attenuation potential is lowest for liquids and highest for air. The ultrasound wavesreturning to the transducer, after being reflected from tissues they encounter, are used to construct atwo-dimensional image based on the time the waves take to return to the transducer (determining thedistance of the reflecting structure from the surface) and the amplitude of returning waves (determiningthe brightness or echo-texture of a given structure). The attenuation coefficients for air and bone are veryhigh, meaning that ultrasound waves cannot form an image for bony or air-filled structures [2].

Ultrasound machines come equipped with different probes that have different sizes/footprints and arecapable of generating specific ranges of ultrasound frequencies. High-frequency ultrasound waves are onlycapable of penetrating shallow structures but with very good image resolution. Low frequency waves areuseful to image deeper structures but with lower image qualities. Examining the chest wall and parietalpleura can be achieved by a high frequency (usually linear) probe which operates with a frequency rangeof 7.5–12 MHz, and is capable of penetrating to depths of 2–5 cm. For imaging deeper structures such as apleural effusion or a lung abnormality, a low frequency probe, which typically has a curvilinear footprint,is more suitable. It generates a frequency range of 2–5 MHz which is capable of penetrating up to a depthof 10–25 cm from the surface of the skin. The latter is the probe most widely used in examining patientswith pleural effusion [3].

Image acquisitionIn order to access the pleural space, the ultrasound beams need to be directed between the ribs, as bonystructures cause complete reflection of ultrasound waves casting shadows and obscuring all deeper tissue.When the ultrasound probe is oriented perpendicular to an intercostal space, two anechoic (black)shadows are created by the bordering ribs and the inside of the chest cavity is only visible from betweenthe ribs (figure 1a). However, by rotating the probe 90° so that its long axis is parallel to the ribs, acomplete image of the pleural space is acquired (figure 1b) by carefully accessing the so-called acousticwindow between the ribs.

ModesThe description above details how the image is formed in the brightness (B)-mode which is also termedthe greyscale due to the different shades of grey that are imparted to tissues according to theirecho-texture. Most of the examination purposes are achieved in this mode, including real-time guidanceduring procedures. Motion (M)-mode is a useful mode during TUS examination which is used to closelyexamine (and quantify) the degree of motion of a specific structure or section of the TUS image. A

TABLE 1 Advantages and pitfalls of using ultrasound in pleural diseases

Advantages Pitfalls

Widely available Operator dependent

Relatively cheap Not suitable for examinations in patients withsubcutaneous emphysema

Mobile – ideal point-of-care test Difficult to examine patients with narrow intercostalspaces (e.g. fibrothorax)

Lack of ionising radiation (making the testsafe to repeat)

Inferior to computed tomography in delineating complexpleural spaces (e.g. multi-loculated hydropneumothorax)

Improves safety of pleural procedures

Allows real-time invasive procedure guidance

More sensitive than computed tomography forpleural fluid characterisation

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movable vertical reference line is used to determine the section of interest in the greyscale picture andonce M-mode is applied, the image is changed to a strip that shows the movement of structures on thisreference line over time. M-mode is a one-dimension image as opposed to the two-dimension imageobtained with the B-mode (figure 2a for M-mode examination of diaphragm movement). Dopplerscanning can be added to the greyscale image for ease of identification of moving fluids, and particularlyblood vessels. This mode applies a colour in the range between red and blue to the vascular structure. Thecolour is determined according to the speed and the direction of the moving blood towards or away fromthe transducer (and does not represent arterial or venous blood) (figure 2b).

AnatomyThe most appropriate position to systematically examine the pleural spaces is to sit the patient upright orslightly leaning forward and to examine them from behind. Both sides should be examined even if theabnormality identified by previous imaging was only on one side. Due to the oblique orientation ofintercostal spaces at the back, the authors prefer to orient the probe upward and laterally to explore thepleural spaces thoroughly. This starts by identifying the space where the diaphragm and underlyingabdominal viscera (the liver and kidney on the right, or the spleen and kidney on the left) are seen. It isthe radiological convention to have the probe oriented so that the structures above the diaphragm are onthe left side of the image with caudal structures on the right. This is for ease of interpretation of storedimages that are reviewed after an examination is finished, and reduces the tendency for error when movingfrom one side to another. Following the identification of the diaphragm, the probe is moved craniallywhile maintaining the same angle to inspect the rest of the hemithorax. This is followed by moving theexamination laterally to the mid-axillary line and anteriorly and repeating the inspection from the lowermost space upwards.

The skin, subcutaneous tissue and intercostal muscles are seen using any probe, although the resolutionand the details are much finer with the linear (high frequency) probe [4]. The intercostal vessels can bevisualised between the intercostal muscles using Doppler. Except for the first and last 6 cm of theircourses, the vessels are usually shielded beneath the lower border of the upper rib in a given space (andhence are not seen by TUS), although variations and tortuosity are occasionally seen, especially in theelderly (figure 2b) [5].

In normal pleura the membranes appear deeper to the intercostal muscles as a single 0.2 mm line (figure 1)that shows in real-time the “sliding” sign; a shimmering movement caused by the gliding of the parietalover the visceral pleura. The underlying lung is not normally visualised as air causes scattering ofultrasound beams, but the presence of pleural fluid (an excellent medium for ultrasound waves’propagation) allows the examination of deeper structures including the collapsed lung. Therefore, it shouldbe noted that the “lung sliding” sign is in fact a sonographic artifact created by the ultrasound waves, anddoes not represent “normal lung” as opposed to anatomical details that can be delineated during ultrasoundexamination of other organs, e.g. the liver or thyroid gland. However, the normal pattern of artifacts can beused to exclude the presence of pathology such as pneumothorax, peripheral lung consolidation orpulmonary oedema.

a) b)

FIGURE 1 a) Thoracic ultrasound using low frequency probe oriented perpendicular to the intercostal spacelong axis. Note how the ribs (arrowheads) cast deep shadows causing interruption to the pleural line (arrows).b) The same image after orienting the probe to remove the rib shadows. Note the continuous pleural line(arrow).

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In the presence of pleural effusion, various characteristics should be evaluated. The size of the effusionshould be noted. Semi-quantitative methods measuring the depth of the effusion and its height in ribspaces usually suffice, but various methods exist for more accurate calculations [6]. The echogenicity(brightness) of the effusion should also be noted, as it gives an indication to its aetiology (figure 3a and b).Echogenic effusions are usually due to exudates [7], although concentrated transudates due to diuretictherapy can appear echogenic [8]. Anechoic effusions can be transudative or exudative. Exudative effusionseither due to infection or malignancy tend to form fibrous septations (figure 3c), which, if present, havevarious diagnostic and therapeutic implications. The presence and extent of such septations should also benoted. The parietal and visceral pleurae should be inspected for thickening or nodularity. The latter ishighly predictive of pleural malignancy [9].

Inspection of the position of the diaphragm, its configuration and mobility and the presence of anythickening or nodularity of its covering pleura is very useful in cases of suspected pleural malignancy(figure 2c) [10]. The diaphragm should appear convex towards the thorax and should descend towards theabdomen during inspiration, a mechanism which can be impaired with large effusions where paradoxicalmovement can occur.

DiagnosisInfectionThe ultrasound echo-texture of an effusion can point to its aetiology. Homogeneously echogenic effusionstend to occur with haemorrhagic pleural effusions and empyema [11]. A less known sonographic sign, the“suspended microbubble sign”, which describes echogenic shadows floating up the ultrasound screen andrepresents gas bubbles is occasionally depicted in purulent pleural collections [12, 13].

b)a)

d)c)

FIGURE 2 a) The upper part of the image is an ultrasound still in B-mode of pleural effusion andhemidiaphragm, with a green line traversing the middle. The lower part of the image corresponds to theM-mode image acquired for the structures traversed by the green line moving over time. Note the wavy whiteline and the +marks pointing to the degree of diaphragm excursion in one respiratory cycle. b) Dopplerexamination showing an unshielded intercostal vessel in the deep part of the chest wall. c) Right pleuraleffusion, collapsed lung and convex thickened hemidiaphragm (arrowhead). Malignancy is confirmed by thepresence of a nodule (arrow) on the diaphragm. d) Under real-time ultrasound guidance a core-cutting needle(arrows) is advanced to biopsy the parietal pleural thickening, the extent of which is indicated by twoarrowheads.

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Pleural aspiration is required to determine the nature of any effusion and, should infection be diagnosed, asmall-bore chest tube will be required. As per the BTS guidelines, both procedures should be done withthe guidance of TUS to ensure a successful and safe procedure [1]. More recently, it has beendemonstrated that obtaining TUS-guided pleural biopsies for microbial cultures on drain insertion forpleural infection improved the microbial yield by 30% in comparison to cultures of pleural fluid alonewithout imparting any increased risk of complications [14]. This technique can be particularly useful inpatients who have received antibiotics prior to sending pleural fluid cultures.

Ultrasound is more sensitive than thoracic computed tomography (CT) in detecting septations in thepleural fluid (figure S1). Extensive septations can complicate the management of pleural infection byimpeding thorough drainage (figure 3c), and may be predictors of failed medical treatment and the needfor management escalation [15, 16]. In these septated effusions, real-time TUS guidance can be used todirect chest drain placement into the largest locule visualised. Knowing that an effusion is multi-septated isalso useful because pleural fluid pH can vary between different locules of fluid which has an importantbearing on the management [17].

MalignancyMesothelioma is the only major primary pleural malignancy. However, the pleura is more commonlyinvolved by malignancy in the setting of metastatic cancer, with lung and breast being the most commonprimaries to metastasise to the pleura [18]. TUS can aid in the diagnosis of pleural malignancy and hasbeen demonstrated to have high specificity for malignancy with certain sonographic features. For pleuralprocedures such as thoracentesis, image-guided pleural biopsies and medical thoracoscopy, which may beneeded to obtain cytological or histological confirmation, TUS is required either for procedural planningor execution (see Procedure guidance section).

TUS can delineate pleural thickening and irregularity and can identify biopsy sites in cases of suspectedmalignancy, even in the absence of a pleural effusion [4]. In cases of malignant pleural effusion (MPE),metastatic pleural nodules >5 mm seen on TUS on the parietal or diaphragmatic pleura is pathognomonicof pleural malignancy (figure 2c) [4]. Other TUS features suggesting malignancy include pleural thickening>1 cm and the presence of hepatic deposits [10]. The combination of the aforementioned sonographiccriteria had a sensitivity of 79% and specificity of 100% for diagnosing pleural malignancy [10]. TUS is

a) b)

c)

FIGURE 3 a) Non-echogenic pleural effusion and part of the collapsed lung. b) Highly echogenic effusion andunderlying diaphragm. c) Complex septated right pleural effusion.

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particularly helpful in this context, as malignant deposits tend to be most extensive nearer to the diaphragmwhich is the region most amenable to TUS examination in the presence of pleural fluid [10, 19].

An additional merit for TUS in malignancy is that infiltration of the pleura or chest wall by thoracicmalignancy is best delineated by TUS that has a sensitivity of 89%, which is much higher than that ofthoracic CT (42%) [20].

A more recent innovation, shear wave elastography, which measures the degree of stiffness of tissue, hasbeen shown to enable differentiation between benign and malignant pleural thickening, where the latterwas found to be stiffer, and to facilitate faster propagation of the elastography waves. Using a specificcut-off for the speed of wave propagation, the sensitivity of identifying malignant pleural disease was83.64% with a specificity of 90.67% [21].

PneumothoraxPneumothorax is the abnormal accumulation of air in the pleural space. It seems counter intuitive thatultrasound beams, which are scattered by air, can be used to diagnose pneumothorax. The sonographicfeatures for diagnosing pneumothorax are based on the disappearance of the normal TUS features seen inthe presence of normally aerated lung when the pleural layers are opposed. Lack of pleural sliding is one ofthe signs suggesting the presence of pneumothorax. Applying M-mode can help in the differentiationbetween present and absent pleural sliding since normal sliding on M-mode exhibits a granular patterndeeper to the pleural line while in the absence of sliding this granular pattern is replaced with multipleparallel hyperechoic lines (the so-called barcode sign). The main caveat with using this sign is that it is notspecific to pneumothorax as sliding can be significantly impaired or absent in conditions such as severeemphysema or following pleural infection or pleurodesis [3, 22]. The most specific TUS sign forpneumothorax is the “lung point”. This is the point where the sliding lung can be seen together with thenon-sliding pleura in the same TUS image and the sliding lung is observed to encroach on the still partand recede again with breathing [22]. In patients with proven pneumothorax, the lung point seen on TUShad a specificity of 100% but with a sensitivity of 66% [23] meaning that the sign is pathognomonic ofpneumothorax, but its absence cannot rule out the condition.

TUS is frequently criticised for having considerable limitations in diagnosing pneumothorax [3, 24]. It canbe particularly difficult to interpret in large air collections as no lung point is identifiable if the lung isfully collapsed and away from the chest wall [25] and lung sliding can be abolished following pleurodesisor when there is lung bullae. However, there is a wealth of literature supporting the use of TUS as apoint-of-care test for patients with suspected pneumothorax in the acute and emergency settings [20]. Twometa-analyses concluded that bedside TUS is more accurate than supine radiography to screen forpneumothorax in trauma patients [26, 27]. Even small pneumothoraces that are not picked up onradiographs are clinically relevant in such patients who are commonly put on positive pressure ventilatorysupport with its risks of increasing the size of pneumothorax and dictating the need for chest drainage [28].Following up these patients can be achieved using TUS which can delineate an enlarging pneumothorax ifthe lung point seen during earlier examination is noticed to move laterally in an intercostal space [29]. Itshould be noted that the size of pneumothorax (as can be easily seen and quantified on a chest radiographfor the purpose of therapeutic choice) is not measurable using TUS, and complex pneumothoraceswhere there is tethered lung requires CT imaging for both delineation and intervention and, therefore, theuse of TUS to diagnose pneumothorax is better reserved for critical situations where waiting to obtain aradiography may not be safe in the emergency department or intensive care units.

Procedure guidancePlanningThe risk of iatrogenic complications or a “dry tap” following blind thoracentesis has long beenacknowledged [30]. In 2008, a safety alert was raised in the UK calling for a change of practice to guardagainst the avoidable complications of blind pleural procedures [3]. The BTS guidelines stronglyrecommend using TUS before procedures involving pleural effusion [1]. Previously, TUS “guidance” forpleural procedures was accomplished by sending the patient for TUS assessment at the Radiologydepartment where the safe point of entry was marked and then the patient was transported back to theward or room where the procedure was to be performed. This so-called “X marks the spot” method wasfound to be associated with an unacceptable risk of iatrogenic pneumothorax [31] due to the inevitablechanges in the patient’s position and the relationship between the effusion position and the skin markfrom when the TUS was performed until the actual execution of the procedure. Thus, it is necessary tominimise any repositioning or time lapse between the TUS examination and the procedure to ensuresuccess of the intervention and maintain patient’s safety [3]. A large nationwide study from the USA

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found that TUS guidance for pleural aspiration resulted in a reduction in the incidence of iatrogenicpneumothorax by 19% in comparison to procedures carried out blindly (OR 0.81, 95% CI 0.74–0.90) [32].

With the widespread availability of competence in TUS by chest physicians, sending a patient with aneffusion to the radiologist for a TUS scan has become uncommon. However, to minimise any potentialharm to patients, cases with small fluid collections that require real-time TUS guidance during theprocedure should be referred to an individual with appropriate experience of conducting such techniques;either an experienced pleural physician or interventional radiologist.

The usual position of the patient for TUS scanning is the sitting position, which is also suitable forthoracentesis that is typically carried out in one of the intercostal spaces at, or very close to, themid-axillary line. With loculated effusions, this position may need to be altered. Patient positioning duringTUS examination is shifted to the lateral decubitis posture for procedures that are carried out in thisposition. This includes pleural biopsies either via medical thoracoscopy or TUS-guided tru-cut needle andindwelling pleural catheter insertion [3, 33].

Conventionally, before a pleural procedure, prior imaging in the form of a chest radiograph or CT scanwill have been performed. A comprehensive TUS mapping of the identified effusion (or any other lesion)is attempted as described above. The point of intervention should preferably be in the mid-axillary line, orat least >6 cm from the spine, to stay away from the unguarded intercostal bundle [34]. Once a spot isidentified for intervention, the authors prefer to screen for a vulnerable intercostal artery using Dopplerscanning (figure 2b) and to avoid, where possible, any point where the artery is in the middle of the spacesince its laceration can potentially lead to serious bleeding [35].

During planning for medical thoracoscopy, TUS should be performed while the patient is on the table as itensures safe entry to the pleural cavity without injury to the underlying lung [36, 37]. Centres with advancedcapabilities in medical thoracoscopy perform pneumothorax induction prior to procedures where there islittle or no pleural effusion. In this situation it is very important to ensure that the lung is not tethered tothe chest wall which means that if air is allowed into the pleural space, the lung will collapse and a space willbe created to enable performing the procedure [33, 37]. TUS is useful in predicting lung tethering byobserving lung sliding [38]. In cases where there is no lung sliding, patients can be triaged to TUS-guidedcore-cutting pleural biopsy while on the table in order to avoid futile and complication ridden attempts toconduct medical thoracoscopy. In a review from a dedicated pleural unit, 5.2% of 252 attempted medicalthoracoscopy procedures over a 4-year period were converted to TUS-guided pleural biopsy due to lack ofsafe TUS features to proceed [39]. Of these converted procedures, 85% provided sufficient tissue fordiagnosis using a TUS cutting needle technique, avoiding a further procedure [39].

Real-time guidanceTUS-guided pleural biopsies are now carried out by chest physicians in several centres around the world whichmeans that fewer procedures are carried out by radiologists and under CT guidance [3, 33]. TUS involvementduring a procedure can be described as assistance (the freehand approach) or guidance (the real-timeapproach). Real-time TUS guidance, where the needle is introduced into tissues and biopsies are taken underfull ultrasound vision (figure 2d) is more time consuming and requires more training and experience.

In the setting of high tuberculosis prevalence (where lesions diffusely affect the pleura), the yield fromTUS-assisted biopsies approach 90% with a very low rate of complications [40]. For suspected pleuralmalignancy, TUS-guided (but not TUS-assisted) pleural biopsies had a diagnostic yield similar toCT-guided biopsies and a better safety profile [39, 41, 42]. The improved safety with TUS guidancecompared to CT is related to the real-time capability of the former which allows for compensation ofrespiratory movements while advancing the needle under vision, ensuring that the pleural surface orthickening is tangentially biopsied [43]. Other advantages include lower cost, shorter procedure times andno exposure to ionising radiation.

As previously mentioned, sliding seen on TUS permits medical thoracoscopy to proceed safely in patientswho require pleural biopsy without having pleural effusion. Moreover, TUS can be used to guide theneedle used to induce pneumothorax, to visualise pneumothorax induction in real-time and to confirmthe formation of pneumothorax before introducing the trocar [44].

Post-procedure complicationsThe authors routinely perform TUS examination following any pleural intervention to screen for anycomplications that may occur early in their course which facilitates appropriate and timely management.Post-intervention bleeding can be noted either on Doppler scanning [45] or occasionally as spreadingechogenic material from the puncture site [46]. Early recognition expedites management and minimises

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the potential for harm to the patient [34]. In addition, TUS is useful as a tool to detect the formation andenlarging of a pneumothorax following interventions in the thorax [25].

PrognosticationSymptomatic benefitPleural fluid accumulation leads to breathlessness and in many, but not all, cases its drainage improvesbreathing. The growing effusion causes compression of the underlying lung together with an increase in thesize of the affected hemithorax which manifests as bulging of the chest wall (due to loss of the pulling forcesof the lung) and flattening or even inversion of the ipsilateral diaphragmatic cupola (figure 4) [47]. Animalstudies have shown that the functional residual capacity of the lung shrinks by only one-third of the volumeof the accumulated fluid [48] and that the rest of the volume of the effusion is accommodated by thedownward displacement of the diaphragm [49]. The abnormal shape of the diaphragm puts it in adisadvantageous point in its length-tension curve which impairs its capacity to generate trans-diaphragmaticpressure in a way similar to that seen in patients with hyperinflation due to emphysema [50]. Thismechanical disadvantage causes dissociation between the neural drive to the diaphragm and the actualtension generated which is responsible for the sensation of significant breathlessness [47].

Diaphragm dysfunction can be observed sonographically as the paradoxical movement of thehemidiaphragm towards the thorax with inspiration [3]. It has been shown that patients whose effusioncauses flattening, diaphragm inversion (figure 4) or paradoxical movement experience considerablesymptomatic improvement following effusion drainage [51]. This means that TUS can be useful incomplex patients who suffer from pleural effusion besides other pathologies that can contribute tobreathlessness (such as lung masses or pulmonary embolism), as identifying distorted diaphragm shapeand movement on TUS means that the effusion is contributing to breathlessness and that draining theeffusion is likely to improve symptoms [3]. However, it should be noted that the opposite is not proven tobe true, i.e. even if the diaphragm is not flat/inverted, thoracentesis may result in symptom improvement.Additionally, if thoracentesis is performed, the aim should be to drain until the diaphragm reverts to itsnormal shape instead of targeting a pre-specified volume.

Non-expandable lungIn patients with large symptomatic MPE, the ability to predict the likelihood of lung re-expansionfollowing complete drainage is beneficial to tailor the most suitable therapeutic option for managing sucheffusions. The lung that does not re-inflate following pleural fluid drainage is termed non-expandable lung(NEL). In the presence of NEL, long-term management of symptomatic MPE should be in the form ofindwelling pleural catheter insertion and not pleurodesis which is not achievable if the two layers of thepleura cannot be brought into apposition. For a long time, the only method available to diagnose NEL wasto perform pleural manometry which entails serial pleural pressure measurements during effusiondrainage [52], or to conduct a large volume thoracentesis and a post-procedure chest radiograph.Manometry is a tedious procedure that is seldom carried out outside research and in a number ofinterested centres. A group of investigators studied the potential use of TUS to predict the presence ofNEL [53]. They looked at the degree of movement and deformation of the collapsed lung secondary toheart beats during breath-hold. Lung movement was measured in the M-mode (figure S2) while lungstrain was measured using the speckle tracking function of echocardiography [53]. The group found thatNEL showed less movement and deformation in comparison to lungs that eventually expanded followingdrainage. Moreover, in the same study, the sensitivities of both methods to predict NEL exceeded that ofpleural manometry [53]. Another group found that the degree of displacement of the collapsed lungmeasured in M-mode could predict incomplete lung re-expansion following medical thoracoscopy [54].

a) b) c)

FIGURE 4 Three images showing the effect of the weight of pleural effusion on the configuration of thecorresponding hemidiaphragm that changes from a) its normal convex shape, b) to be flattened and c) withlarger effusions becoming inverted.

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This is a promising technique that can become a simple and noninvasive tool in predicting whether thelung would re-expand following intervention. The information gained from the technique that can beeasily performed by chest physicians could inform the discussion between the clinician and the patientregarding the management plan and the possible therapeutic options.

Pleurodesis successPleurodesis is the application of an injurious substance into the pleura with the aim of causing symphysisof the two layers and obliteration of the potential space between them. This is most commonly carried outin MPE or in recurrent pneumothorax [55]. Given that sliding is a TUS sign caused by gliding of thepleural membranes, pleurodesis intuitively is expected to abolish this sign. This was tested in patients withpneumothorax who underwent surgical pleurodesis either by pleurectomy or pleural abrasion. Theinvestigators found that 3 weeks after surgery, pleural sliding as assessed by TUS was abolished in all chestregions in patients who underwent pleurectomy and in most of the chest regions in those who had pleuralabrasion [56]. In an animal study, the lack of pleural sliding on TUS was strongly correlated withmacroscopic and microscopic pleural symphysis in pigs with artificial pneumothorax exposed to talcpleurodesis [57]. In a recent case series of patients with MPE who underwent talc slurry pleurodesis, aTUS pleural adherence score obtained 24 h post-pleurodesis could predict effusion recurrence [58]. TheSIMPLE randomised trial is currently enrolling to further assess the role of TUS in outcome prediction ofpleurodesis and whether its use can expedite the decision for chest tube removal and discharge in patientswith MPE by studying the pattern of pleural sliding before and after pleurodesis [59].

Another sonographic feature that has been recently studied as an outcome predictor for talc pleurodesissuccess in patients with MPE is the echo-texture of the pleural effusion. The presence of echogenicswirling, a finding that is commonly seen in MPE [60], was associated with lower incidence of pleurodesissuccess when compared to effusions that lack this feature [61].

Conclusions and future directionsThe introduction and widespread use of TUS as a point-of-care test has revolutionised the management ofpleural diseases. A once diagnostic tool for detection of pleural effusion only, the uses of TUS in pleuraldiseases have expanded to include various diagnostic and therapeutic indications enhancing the accuracyof diagnosis and refining treatment decisions. Further work is ongoing to explore the potential use of TUSfor prognostication in different pleural diseases. Newer techniques are emerging such as elastography andcontrast-enhanced TUS and current research is looking at its role in differentiating benign from malignantpleural disease and whether it can be used to direct biopsy sites in cases of suspected thoracic malignancy.

Author contributions: M. Hassan conceived the report and prepared the first draft. All authors contributed in datacollection. R.M. Mercer and N.M. Rahman critically reviewed the draft and bibliography. All authors reviewed andagreed to the final manuscript.

Conflict of interest: None declared.

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